Large‐scale movement patterns in a social vulture are influenced by seasonality, sex, and breeding region

Abstract Quantifying space use and segregation, as well as the extrinsic and intrinsic factors affecting them, is crucial to increase our knowledge of species‐specific movement ecology and to design effective management and conservation measures. This is particularly relevant in the case of species that are highly mobile and dependent on sparse and unpredictable trophic resources, such as vultures. Here, we used the GPS‐tagged data of 127 adult Griffon Vultures Gyps fulvus captured at five different breeding regions in Spain to describe the movement patterns (home‐range size and fidelity, and monthly cumulative distance). We also examined how individual sex, season, and breeding region determined the cumulative distance traveled and the size and overlap between consecutive monthly home‐ranges. Overall, Griffon Vultures exhibited very large annual home‐range sizes of 5027 ± 2123 km2, mean monthly cumulative distances of 1776 ± 1497 km, and showed a monthly home‐range fidelity of 67.8 ± 25.5%. However, individuals from northern breeding regions showed smaller home‐ranges and traveled shorter monthly distances than those from southern ones. In all cases, home‐ranges were larger in spring and summer than in winter and autumn, which could be related to difference in flying conditions and food requirements associated with reproduction. Moreover, females showed larger home‐ranges and less monthly fidelity than males, indicating that the latter tended to use the similar areas throughout the year. Overall, our results indicate that both extrinsic and intrinsic factors modulate the home‐range of the Griffon Vulture and that spatial segregation depends on sex and season at the individual level, without relevant differences between breeding regions in individual site fidelity. These results have important implications for conservation, such as identifying key threat factors necessary to improve management actions and policy decisions.


| INTRODUC TI ON
Animal movements are a consequence of an organism's internal state (e.g., sex, age, breeding stage) and environmental factors (e.g., food availability or weather), and can affect individual fitness and ecological processes at local and global scales (Hansson et al., 2014).
Individual movements are also influenced by inter and intraspecific relationships (e.g., competition), which may lead to spatial compartmentalization and the maintenance of population-specific movement patterns over time (Nathan et al., 2008). Deciphering how these factors modulate individual movements and how the latter are compartmentalized in space and time is essential to understanding population dynamics (Costa-Pereira et al., 2022) and identifying priority areas for conservation and management (Katzner & Arlettaz, 2020).
Home-range size and cumulative distance traveled are key elements in the study of animal movement ecology (Kie et al., 2010;Shaw, 2020;Thaker et al., 2019;Tucker et al., 2018), defining foraging patterns at the individual and population-level, and assessing their stability over time (e.g., Shaffer et al., 2017). griffon vulture, home-range, scavenger, site fidelity, spatial segregation
Vultures from the Gyps genus (which includes seven species) are among the largest flying birds, showing high sociality and covering large areas in search of ephemeral and unpredictable resources such as carrion (e.g., 162,824 km 2 annually on average in the case of Cape Vultures, Gyps coprotheres; Jobson et al., 2021).
In this paper, we gather movement data from 127 GPS-tagged We hypothesize that adult Griffon Vultures, being a large monomorphic colonial species, will exhibit large home-ranges and will travel long distances to fulfill their requirements (mainly food), especially during the autumn and winter, when food availability is the lowest Spiegel et al., 2013). We also predict that the fidelity of monthly home-ranges should be similar between sexes due to the lack of dimorphism, but would differ between seasons, as foraging constraints are more likely during the breeding period (see Carrete & Donázar, 2005). Finally, we expect differences between breeding regions due to differences in resource availability . Birds were trapped using remotely activated cannon nets and cage traps baited with livestock carcasses. Individuals were tagged with yellow or blue plastic alphanumeric and metal rings and equipped with solar-powered GPS/GSM transmitters (Ecotone https://ecoto ne-telem etry.com/en, Ornitela https://www.ornit ela.com/, and e-Obs https://e-obs.de/). Devices were attached using a Teflon tape backpack harness. The total weight of the transmitters and rings did not exceed 64 g, which represented less than 3% of the body weight of the individuals (Bodey et al., 2018). The age of individuals was estimated from plumage molt and other external features such as the color of the culmen and the eyes (Donázar, 1993;Zuberogoitia et al., 2013), while sex was determined using molecular sexing techniques from body feather samples (Fridolfsson & Ellegren, 1999).

| Capture and tagging of vultures
Tracking devices were programmed to record fixes (i.e., GPS positions) at 5-10-min intervals from 1 h before sunrise to 1 h after sunset (see Table 1 for details of the tracking devices and sampling frequency). GPS data were incorporated into the Movebank online data repository (www.moveb ank.org). Data were standardized by resampling the GPS fixes to 15 min for each individual to homogenize our dataset. Vultures were tracked on average 1040 ± 809 days with a mean number of fixes per individual of 41,335 ± 40,493.

| Estimation of home-range, cumulative distance traveled, and site fidelity
We estimated annual and monthly home-ranges using the 95% kernel density estimator contours (KDE) and the cumulative distance traveled for each tagged individual using the "amt" package (Signer et al., 2019). We selected KDE function instead of AKDE since this had no qualitative improvement to our results and notably increased computational time compared to KDE function (see for instance Silva et al., 2022). Cumulative distance traveled per month was measured as the total length of each track (in km) (Edelhoff et al., 2016). Individuals with less than ten fixes per day were discarded (n = 4 cases).
We measured the individual home-range fidelity by calculating the percentage of overlap between consecutive monthly homerange (Fieberg & Kochanny, 2005). We selected the 95% KDE as an estimator of home-range to evaluate differences in foraging areas.
The percentage of overlap was quantified using the Bhattacharyya coefficient, which ranges between 0 (complete segregation) and

| Data analysis
We analyzed the effect of sex, season, and breeding regions on the monthly home-range sizes, cumulative monthly distances traveled (normal error distribution, identity link function), and percentage F I G U R E 1 Movements and nest locations of 127 GPS-tagged adult Griffon Vultures in northern (Alto Ebro and Pyrenees), central (Segovia), and southern (Cádiz and Cazorla) Spain. N represents the number of tagged vultures for each breeding region. Photo credit: Manuel de la Riva.

Home-range (km 2 )
Cumulative distance traveled ( of monthly overlap (beta error distribution, identity link function) using generalized linear mixed models (GLMMs; glmmTMB package, Brooks et al., 2017). Sex, season, and breeding region were included as fixed factors, while individual identity and year were included as random terms in the models to avoid pseudo replication.
We did not divide the period into breeding stages since we could not rule that all individuals were breeding each monitoring year and, therefore, followed the same breeding cycle periods. Instead, we here referred to the season as the division of the year based on changes in weather, ecology, and the number of daylight hours in a given region. In the case of the breeding region, we regard this variable, not only as an indicator of differences in the periods suitable for soaring (mediated by photoperiod; see Scacco et al., 2019) but also as a potential proxy of differences in the food available in the field (e.g., some regions encompass much more carrion than others in absolute numbers; Morant et al., 2022) and population differences in the levels of exposure to known threats (i.e., risk of collision, electrocution or poisoning; Arrondo, Sanz-Aguilar, et al., 2020).
Finally, we did not consider the interaction between the aforementioned variables due to (1) the complexity of the understanding that is implicit to them (e.g., sex differences in movement associated with particular regional conditions) and (2) to avoid speculations without any empirical foundations in the interpretation of the results.
Models were compared using the Akaike Information Criterion corrected for small sample sizes (AICc; Burnham & Anderson, 2002).
The best model was the one with the lowest AICc value. All models with a difference of ΔAICc < 2 were considered alternatives (Burnham & Anderson, 2002). For the best model, homogeneity of variance and normality of residuals was inspected by using the "ggresid" package to check the goodness-of-fit of our best models (Goode & Rey, 2019). We estimated the variance explained by TA B L E 2 Models obtained to assess the effects of individual sex, season, and population on the movement and spatial segregation patterns of 127 GPS-tagged adult Griffon Vultures in Spain. the fixed and random factors by using the "performance" package (Lüdecke et al., 2021), while differences between their levels were assessed through Tukey's post hoc tests using the "emmeans" package (Lenth, 2022). All tests were two-tailed, statistical significance was set at α =0.05, and all results were shown as mean ± standard deviation. Results of the Tukey's post hoc tests included the marginal means and its standard error. Spatial and statistical analyses were done in R version 4.0.3 (R Core Team, 2021).

| RE SULTS
Griffon Vultures exploited very large annual home-range sizes (ca. 5000 km 2 ), showing average monthly cumulative distances traveled of 1776 km (Table 1), and a monthly home-range fidelity of 67.77 ± 25.05%. Monthly home-ranges differed between sexes, seasons, and breeding regions (Tables 2 and 3; Figure 2). Males showed a smaller monthly home-range size than females ( Table 3). Birds also showed larger home-ranges during spring and summer compared to autumn and winter (Table S2; Figure 2). Individuals from southern breeding regions (Cazorla, Cádiz), and central Pyrenees showed, on average, larger home-ranges than those of central (Segovia) and northern breeding regions (Alto Ebro) (Table S2 and Figure 2).
Monthly cumulative distances traveled were similar for both females and males (Tables 2 and 3; Figure 3). However, birds traveled longer distances during spring and summer than during autumn and winter (Table S2). Individuals from Alto Ebro, Segovia, and Pyrenees traveled larger monthly distances than those of Cazorla and Cádiz (Table S2; Figure 3).
The monthly home-range fidelity was slightly higher for males than females, and during spring and summer, being the lowest in autumn and winter. Likewise, there were differences in fidelity between breeding regions. Individuals from Central Spain (Segovia) showed higher fidelity over time than those from the north (Alto Ebro, Pyrenees) and southern Spain (Cádiz, Cazorla) ( Tables 2 and 3 and Table S2; Figure 4).

TA B L E 3
Estimates for fixed terms of the best models of monthly home-range size, cumulative distance traveled per month and monthly home-range fidelity for 127 GPS-tagged adult Griffon Vultures in Spain. Note: Season, Sex, and Breeding region variables were coded as a factor, being "Winter," "Female," and "Alto Ebro" the reference values for statistical comparisons. Significant values are highlighted in bold.

Response variable Predictors
Abbreviation: SE, Standard error.
Griffon Vulture movements varied between seasons, breeding regions and sexes. We found that movements were larger during spring and summer, which is similar to other soaring raptors such as Bearded Vulture or Bonelli's Eagle (see Margalida et al., 2016;Pérez-García et al., 2013). This could be related to the food requirements associated with reproduction, which may force vultures to prospect larger areas, seeking for dispersed and unpredictable carcasses to satisfy the food requirements of the offspring and themselves (Carrete & Donázar, 2005). However, seasonal differences could be also explained by longer days (and therefore more time to forage) and better atmospheric conditions particularly during summer, minimizing energy expenditure during long-range movements (see Martin-Díaz et al., 2020). Similarly, differences in monthly home-range size and cumulative distance traveled between regions could be explained by differences in both the importance of predictable and nonpredictable food availability and the ability to move due to better flight conditions due to the presence of thermal uplifts (Scacco et al., 2021). For instance, the southern populations may experience a higher thermal uplift availability (mainly due to warmer climatic conditions in summer), thus minimizing the energy expenditure while increasing the movement capacity of birds (e.g., see Scacco et al., 2019).
Differences in foraging performance between sexes are common in mammals and birds and are often due to differences in body size and parental duties (Lewis et al., 2002), In monomorphic species such as the Griffon Vulture, these differences might be associated with energetic and nutritional requirements for reproduction (Bennison et al., 2022;Pinet et al., 2012). Our results showed that females have larger home-ranges and travel farther than males. on predictable resources such as supplementary feeding stations or vulture restaurants, while females may rely on more ephemeral and less clumped food resources. Thus, there may be parallel strategies in the large-scale exploitation of space and, therefore, sexual spatial segregation (see also Perrig et al., 2021). Alternatively, the fact that males show a greater fidelity of their monthly homeranges throughout the year and that it is higher during the springsummer period could be related to their greater territoriality. Males may be more involved in nest building and guarding (Xirouchakis & Mylonas, 2007), which might be a response to competence for nesting sites (see Zuberogoitia et al., 2018). Interestingly, females not only showed higher extension of home-ranges than males but also exhibited lower site fidelity. All this reinforces the argument that females might forage more in different locations throughout the year, therefore, showing lesser home-range fidelity over time than males. These sex and seasonal differences in individual home-range fidelity were similar between breeding regions except in the case of Cádiz and Segovia, where females exhibited lower fidelity during spring/summer.

Differences (or lack of them) between breeding regions in indi-
vidual movement patterns indicate that local effects not explored in this work may be affecting them. This is evidenced by the low variance explained by the fixed factors of the best models and the high variance explained by random factors (e.g., home-range size fidelity models). The latter indicates that high interindividual differences in home-range area and fidelity exist. Moreover, there are variables, such as distance to trophic resources, colony size, or habitat type, that perhaps could improve the results from our models and better explain breeding region level differences in the evaluated parameters (see Cecere et al., 2018;Delgado-González et al., 2022;Harel et al., 2017). Finally, it should be taken into account that the effect of differences in the sampling duration of individuals of some breeding regions also affects the observed home-range sizes which may have led to an underestimation of this and other parameters such as cumulative distance or home-range fidelity.

| CON CLUDING REMARK S
Our work adds evidence to the spatial requirements of large soaring birds such as vultures, and the importance of individual and regional differences in explaining their movement patterns. Contrary to our expectations, we found sex-dependent spatial segregation in this monomorphic species, maybe related to behavioral differences between males and females, particularly during the breeding period.
Moreover, we observed that vultures showed larger home-ranges terindividual differences in optimal foraging, and on the intrinsic and extrinsic factors operating at multiple levels (Williams & Safi, 2021).
Beyond this, increasing our knowledge of how these patterns translate into regional differences (or lack thereof) is crucial in predicting population dynamics through movement ecology (Shaw, 2020).
Importantly, our results add information that is crucial may be decisive for the effective management and conservation of highly mobile species which require protective measures to be implemented at large spatial scales. For example, differences in the home-range sizes between females and males may indicate different levels of exposure to well-known threats to species (e.g.,  Pérez-García: Conceptualization (equal); data curation (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); supervision (equal); validation (equal); writing -original draft (equal); writing -review and editing (equal).

ACK N OWLED G M ENTS
We thank all the collaborators involved in the field work and the Program2021_1073, both from Junta de Andalucía. We also thank Louis W. Phipps for the language revision of the manuscript.

CO N FLI C T O F I NTE R E S T S TATE M E NT
The authors declare no competing interests.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data and scripts used in the analyses are publicly available at Zenodo data repository (https://doi.org/10.5281/zenodo.7500857).